Fausto Caruana

When pliers become fingers in the monkey motor system

The capacity to use tools is a fundamental evolutionary achievement. Its essence stands in the capacity to transfer a proximal goal (grasp a tool) to a distal goal (e.g., grasp food). Where and how does this goal transfer occur? Here, we show that, in monkeys trained to use tools, cortical motor neurons, active during hand grasping, also become active during grasping with pliers, as if the pliers were now the hand fingers. This motor embodiment occurs both for normal pliers and for “reverse pliers,” an implement that requires finger opening, instead of their closing, to grasp an object. We conclude that the capacity to use tools is based on an inherently goal-centered functional organization of primate cortical motor areas.

Representation of Goal and Movements without Overt Motor Behavior in the Human Motor Cortex: A Transcranial Magnetic Stimulation Study

We recorded motor-evoked potentials (MEPs) to transcranial magnetic stimulation from the right opponens pollicis (OP) muscle while participants observed an experimenter operating two types of pliers: pliers opened by the extension of the fingers and closed by their flexion (“normal pliers”) and pliers opened by the flexion of the fingers and closed by their extension (“reverse pliers”). In one experimental condition, the experimenter merely opened and closed the pliers; in the other, he grasped an object with them. In a further condition, the participants imagined themselves operating the normal and reverse pliers. During the observation of actions devoid of a goal, the MEP amplitudes, regardless of pliers used, reflected the muscular pattern involved in the execution of the observed action. In contrast, during the observation of goal-directed actions, the MEPs from OP were modulated by the action goal, increasing during goal achievement despite the opposite hand movements necessary to obtain it. During motor imagery, the MEPs recorded from OP reflected the muscular pattern required to perform the imagined action. We propose that covert activity in the human motor cortex may reflect different aspects of motor behavior. Imagining oneself performing tool actions or observing tool actions devoid of a goal activates the representation of the hand movements that correspond to the observed ones. In contrast, the observation of tool actions with a goal incorporates the distal part of the tool in the observers body schema, resulting in a higher-order representation of the meaning of the motor act.

Emotional and Social Behaviors Elicited by Electrical Stimulation of the Insula in the Macaque Monkey

Evidence from a large number of brain imaging studies has shown that, in humans, the insula, and especially its anterior part, is involved in emotions and emotion recognition. Typically, however, these studies revealed that, besides the insula, a variety of other cortical and subcortical areas are also active. Brain imaging studies are correlative in nature, and, as such, they cannot give indications about the necessary contribution of the different centers involved in emotions. In the present study, we aimed to define more clearly the role of the insula in emotional and social behavior of the monkey by stimulating it electrically. Using this technique, one may determine whether direct activation of the insula can produce specific emotional or social behaviors and exactly which parts of this structure are responsible for these behaviors. The results showed that two emotional behaviors, a basic one (disgust) and a social one (affiliative state), were easily elicited by electrical stimulation of specific parts of the insula. Both behaviors were characterized by specific motor and vegetative responses and by a dramatic change in the monkeys responsiveness to external stimuli.

Responses of mirror neurons in area F5 to hand and tool grasping observation

Mirror neurons are a distinct class of neurons that discharge both during the execution of a motor act and during observation of the same or similar motor act performed by another individual. However, the extent to which mirror neurons coding a motor act with a specific goal (e.g., grasping) might also respond to the observation of a motor act having the same goal, but achieved with artificial effectors, is not yet established. In the present study, we addressed this issue by recording mirror neurons from the ventral premotor cortex (area F5) of two monkeys trained to grasp objects with pliers. Neuron activity was recorded during the observation and execution of grasping performed with the hand, with pliers and during observation of an experimenter spearing food with a stick. The results showed that virtually all neurons responding to the observation of hand grasping also responded to the observation of grasping with pliers and, many of them to the observation of spearing with a stick. However, the intensity and pattern of the response differed among conditions. Hand grasping observation determined the earliest and the strongest discharge, while pliers grasping and spearing observation triggered weaker responses at longer latencies. We conclude that F5 grasping mirror neurons respond to the observation of a family of stimuli leading to the same goal. However, the response pattern depends upon the similarity between the observed motor act and the one executed by the hand, the natural motor template.

The neural basis of human tool use

In this review, we propose that the neural basis for the spontaneous, diversified human tool use is an area devoted to the execution and observation of tool actions, located in the left anterior supramarginal gyrus (aSMG). The aSMG activation elicited by observing tool use is typical of human subjects, as macaques show no similar activation, even after an extensive training to use tools. The execution of tool actions, as well as their observation, requires the convergence upon aSMG of inputs from different parts of the dorsal and ventral visual streams. Non-semantic features of the target object may be provided by the posterior parietal cortex (PPC) for tool-object interaction, paralleling the well-known PPC input to anterior intraparietal (AIP) for hand-object interaction. Semantic information regarding tool identity, and knowledge of the typical manner of handling the tool, could be provided by inferior and middle regions of the temporal lobe. Somatosensory feedback and technical reasoning, as well as motor and intentional constraints also play roles during the planning of tool actions and consequently their signals likewise converge upon aSMG. We further propose that aSMG may have arisen though duplication of monkey AIP and invasion of the duplicate area by afferents from PPC providing distinct signals depending on the kinematics of the manipulative action. This duplication may have occurred when Homo Habilis or Homo Erectus emerged, generating the Oldowan or Acheulean Industrial complexes respectively. Hence tool use may have emerged during hominid evolution between bipedalism and language. We conclude that humans have two parietal systems involved in tool behavior: a biological circuit for grasping objects, including tools, and an artifactual system devoted specifically to tool use. Only the latter allows humans to understand the causal relationship between tool use and obtaining the goal, and is likely to be the basis of all technological developments.

Functional organization of the insula and inner perisylvian regions

In the last few years, the insula has been the focus of many brain-imaging studies, mostly devoted to clarify its role in emotions and social communication. Physiological data, however, on which one may ground these correlative findings are almost totally lacking. Here, we investigated the functional properties of the insular cortex in behaving monkeys using intracortical microstimulation. Behavioral responses and heart rate changes were recorded. The results showed that the insula is functionally formed by two main subdivisions: (i) a sensorimotor field occupying the caudal–dorsal portion of the insula and appearing as an extension of the parietal lobe; and (ii) a mosaic of orofacial motor programs located in the anterior and centroventral insula sector. These programs show a progressive shift from dorsally located nonemotional motor programs (ingestive activity) to ventral ones laden with emotional and communicative content. The relationship between ingestive and other behaviors is discussed in an evolutionary perspective.

Seven years of recording from monkey cortex with a chronically implanted multiple microelectrode

A brush of 64 microwires was chronically implanted in the ventral premotor cortex of a macaque monkey. Contrary to common approaches, the wires were inserted from the white matter side. This approach, by avoiding mechanical pressure on the dura and pia mater during penetration, disturbed only minimally the cortical recording site. With this approach isolated potentials and multiunit activity were recorded for more than 7 years in about one-third of electrodes. The indirect insertion method also provided an excellent stability within each recording session, and in some cases even allowed recording from the same neurons for several years. Histological examination of the implanted brain region shows only a very marginal damage to the recording area. Advantages and problems related to long-term recording are discussed.

Four-dimensional maps of the human somatosensory system

Significance Here, we show how anatomical and functional data recorded from patients undergoing stereo-EEG can be combined to generate highly resolved four-dimensional maps of human cortical processing. We used this technique, which provides spatial maps of the active cortical nodes at a millisecond scale, to depict the somatosensory processing following electrical stimulation of the median nerve in nearly 100 patients. The results showed that human somatosensory system encompasses a widespread cortical network including a phasic component, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, as well as a tonic component, centered on the opercular and insular areas, lasting more than 200 ms. A fine-grained description of the spatiotemporal dynamics of human brain activity is a major goal of neuroscientific research. Limitations in spatial and temporal resolution of available noninvasive recording and imaging techniques have hindered so far the acquisition of precise, comprehensive four-dimensional maps of human neural activity. The present study combines anatomical and functional data from intracerebral recordings of nearly 100 patients, to generate highly resolved four-dimensional maps of human cortical processing of nonpainful somatosensory stimuli. These maps indicate that the human somatosensory system devoted to the hand encompasses a widespread network covering more than 10% of the cortical surface of both hemispheres. This network includes phasic components, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, and tonic components, centered on opercular and insular areas, and involving human parietal rostroventral area and ventral medial-superior-temporal area. The technique described opens new avenues for investigating the neural basis of all levels of cortical processing in humans.

Human cortical activity evoked by gaze shift observation: An intracranial EEG study

While is widely accepted that the posterior temporal region is activated during the observation of faces showing gaze shifts, it is still unclear whether its activity is stronger while observing direct or averted gaze. Furthermore, despite its assessed role in social cognition, studies describing an enhanced activity of the posterior temporal region during the observation of gaze aversion interpreted this activity in terms of spatial attention toward the target direction. This spatial attention interpretation is not easily reconcilable with the role of the posterior temporal region in social cognition, and an overarching view of its global cognitive function would be much more preferable. Here we used intracranial EEG to assess the precise spatial localization of the gaze shifts coding in the posterior temporal region, to assess its selectivity for direct versus averted gaze and to distinguish between a spatial‐attentional and a social interpretations of gaze aversion. We found stronger activation during gaze aversion than direct gaze and lateral side switch observation, the latter indicating that the crucial aspect of gaze aversion is the prior presence of the eye contact and its interruption, and not the gaze direction. These results suggest a more social‐oriented interpretation based on the view that among humans, gaze aversion signals a negative relational evaluation in social interaction. Hum Brain Mapp 35:1515–1528, 2014.

A shared neural network for emotional expression and perception: An anatomical study in the macaque monkey

Over the past two decades, the insula has been described as the sensory “interoceptive cortex”. As a consequence, human brain imaging studies have focused on its role in the sensory perception of emotions. However, evidence from neurophysiological studies in non-human primates have shown that the insula is also involved in generating emotional and communicative facial expressions. In particular, a recent study demonstrated that electrical stimulation of the mid-ventral sector of the insula evoked affiliative facial expressions. The present study aimed to describe the cortical connections of this “affiliative field”. To this aim, we identified the region with electrical stimulation and injected neural tracers to label incoming and outgoing projections. Our results show that the insular field underlying emotional expression is part of a network involving specific frontal, cingulate, temporal, and parietal areas, as well as the amygdala, the basal ganglia, and thalamus, indicating that this sector of the insula is a site of integration of motor, emotional, sensory and social information. Together with our previous functional studies, this result challenges the classic view of the insula as a multisensory area merely reflecting bodily and internal visceral states. In contrast, it supports an alternative perspective; that the emotional responses classically attributed to the insular cortex are endowed with an enactive component intrinsic to each social and emotional behavior.